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Exceptional Preservation Reveals Gastrointestinal Anatomy And www.nature.com/scientificreports OPEN Exceptional preservation reveals gastrointestinal anatomy and evolution in early actinopterygian Received: 30 September 2015 Accepted: 25 November 2015 fishes Published: 06 January 2016 Thodoris Argyriou1, Marcus Clauss2, Erin E. Maxwell3, Heinz Furrer1 & Marcelo R. Sánchez- Villagra1 Current knowledge about the evolutionary morphology of the vertebrate gastrointestinal tract (GIT) is hindered by the low preservation potential of soft tissues in fossils. Exceptionally preserved cololites of individual †Saurichthys from the Middle Triassic of Switzerland provide unique insights into the evolutionary morphology of the GIT. The GIT of †Saurichthys differed from that of other early actinopterygians, and was convergent to that of some living sharks and rays, in exhibiting up to 30 turns of the spiral valve. Dissections and literature review demonstrate the phylogenetic diversity of GIT features and signs of biological factors that influence its morphology. A phylogenetically informed analysis of a dataset containing 134 taxa suggests that body size and phylogeny are important factors affecting the spiral valve turn counts. The high number of turns in the spiral valve of †Saurichthys and some recent sharks and rays reflect both energetically demanding lifestyles and the evolutionary histories of the groups. The anatomy of the vertebrate gastrointestinal tract (GIT) reflects many aspects of organismal biology, including diet and feeding habits and hence trophic position, nutrient uptake capabilities, osmoregulation and metabolism1,2. Although a broad evolutionary perspective on the digestive system has been achieved by studying the distribu- tion of the GIT morphologies in extant vertebrates1–3, much information is missing due to the vast proportion of vertebrate animals that are now extinct. This is especially true for actinopterygians (ray-finned fishes), the most speciose group of vertebrates4,5. Whereas GIT diversity of derived actinopterygians (teleosts) is well documented, this is not the case for the non-teleostean actinopterygians, which are represented in the modern fauna by a few depauperate lineages: bichirs and reedfish (two genera and 16 species), sturgeons and paddlefishes (five genera and 27 species), gars (two genera and seven species) and the bowfin (one species)4. These taxa exhibit plesiomorphic GIT morphologies, including the presence of a spiral valve in the posterior part of the intestine (also known as the spiral or valvular intestine) that are reminiscent of those seen in living chondrichthyans and differ from those of teleosts2,3,6. The spiral valve is formed by the intestinal mucosa and submucosa and resembles a spiral staircase extending along part of the length of the posterior mid-gut3,6. This structure differentiates in ontogeny as an invagination of the intestinal epithelium. The resulting crest, due to significant posteroanterior growth, twists around the median axis of the intestine forming successive spirals3,6,7. In several taxa, the initial crest wraps around the median axis of the intestine forming the “scroll valve”3,6,7. A spiral or scroll valve in the posterior part of the intestine is a plesiomor- phic feature shared amongst chondrichthyans (including most “†acanthodians”), non-teleostean actinopterygians, non-tetrapod sarcopterygians (including extant lungfishes that possess a spiral valve and extant coelacanths that possess a scroll valve) and likely “†placoderms”8. The presence of a scroll valve has also been suggested for some early Paleozoic jawless vertebrates9,10 whereas modern lampreys, but not hagfishes, also exhibit a reduced spiral valve3,6. The spiral valve is clearly a character that appeared very early in the evolution of vertebrates. 1Paleontological Institute and Museum, University of Zurich, 8006 Zurich, Switzerland. 2Clinic for Zoo Animals, Exotic Pets and Wildlife, Vetsuisse Faculty, University of Zurich, 8057 Zurich, Switzerland. 3Stuttgart State Museum of Natural History, 70191 Stuttgart, Germany. Correspondence and requests for materials should be addressed to T.A. (email: [email protected]) SCIENTIFIC REPORTS | 6:18758 | DOI: 10.1038/srep18758 1 www.nature.com/scientificreports/ Most paleontological perspectives on the vertebrate GIT are based on indirect evidence from fossilized faeces (coprolites)11 because the corresponding soft tissues are highly susceptible to decay and early loss during fossiliza- tion12. Stomach contents can provide some insights into GIT morphology but have been historically used for tracing feeding habits and trophic positions of extinct organisms13. In rare cases, internal casts of the GIT, deriving from fossilized chyme and/or faecal matter and termed “cololites”14, are preserved in the fossil record11. Cololite studies are scarce, mostly because GIT casts associated with taxonomically recognizable individuals are rarely preserved8,15 (see also Supplementary Table 1 for additional references). Cololites can reflect the gross morphology of the GIT and can provide insights into the biology and phylogeny of the studied organisms. †Saurichthyids, known from latest Permian to Early Jurassic deposits worldwide, were highly specialized, predatory, non-neopterygian actinopterygians that shared an elongate body, an elongated preorbital region and posteriorly situated median fins16–18. Recent phylogenetic analyses consistently place †Saurichthys, the most salient genus of this “family”, as closely related to or part of the chondrostean clade and, often, close to the Triassic fish †Birgeria19–22 (but see ref. 19: Fig. 9A for an alternate placement of †Saurichthys). As for most fossil organisms, little is known about the soft tissue anatomy of †Saurichthys16,23. Here, we provide the first detailed description of cololites from Middle Triassic species of †Saurichthys that constitute a rare and key source of data for studying the evolution of the GIT in early actinopterygians and fishes in general. The striking dissimilarity of the GIT morphology of †Saurichthys, and markedly that of its spiral intestine, to that of extant actinopterygians raises some paleobiological questions. We review the distribution of different morphologies of the GIT across extant and extinct fishes (including elasmobranchs, sarcopterygians and actinopterygians) in order to trace factors including body size, diet, lifestyle and phylogeny that may correlate with different GIT morphologies. Results †Saurichthys costasquamosus. Specimen MCSN 5696 (Fig. 1a,b) is an almost complete individual, only missing the anterior half of its rostrum. Total Length (TL) is slightly over 30 cm and thus smaller than the maxi- mum known size for this species (up to 83 cm)23. Fossilized gut contents span almost the entire Abdominal Cavity Length (ACL). A complete individual of an early actinopterygian (cf. †Luganoia) is preserved as undigested prey in the abdominal cavity just posterior to the head. The prey occupies almost 40% of the ACL (25 vertebral seg- ments16), was swallowed head first, and is arranged in an almost straight, uncoiled manner, reflecting the anatomy of the containing GIT chamber. The contained prey, due to its size, bulges out to the venter of the abdominal cavity of the predator. The distensibility of this GIT segment suggests that it is a true straight stomach rather than a pseudogaster (stomach-like thickening of the midgut seen in some agastric species)2,6,13. Posterior to the head of the prey fish, the GIT chamber tapers and leads to an amorphous digestal cloud that corresponds topologically to the pyloric caeca. However, this structure does not exhibit any morphological (e.g., vermiform) patterns expected of pyloric caeca. We attribute its formation to tearing of the anterior intestine. Posterior to the digestal cloud, the substantial part of the three-dimensional cololite is observed. It measures 36.7 mm in length (23.3% of the ACL), 3.2 mm in height and spans 15 vertebral segments (30 neural arch-like elements16). The surface of the cololite was secondarily smoothened but several visible constrictions indicate the presence of a spiral valve that formed more than 17 turns. No gut infilling was preserved in the area between the end of the cololite and the anal opening. At least part of this empty area was presumably occupied by the rectum. †Saurichthys macrocephalus. The body of PIMUZ T 3916 is coiled in an S-shape and its head is detached23 (Fig. 1c). The TL is approximately 24 cm and, thus, smaller than the maximum TL for this species (66 cm, PIMUZ T 5631). Much of the GIT is well-preserved as a flattened white ribbon within the abdominal cavity23 (Fig. 1c, S1). Visible divisions of the GIT include the putative stomach, a short anterior intestine and part of the spiral intestine (Fig. 1d). The posterior end is obstructed by the pelvic bones, the ventrolateral scale row, and by a small cloud of faecal matter that likely escaped from the intestine after the latter was ruptured. We refer to the straight and somewhat thickened part of the GIT, connecting the oesophagus to the anterior intestine, as the “stomach”. The absence of any sign of a pyloric valve, separating the “stomach” from the intestine, allows us to only tentatively identify a division between the two (Fig. 1c,d, S1). The preserved part of the “stomach” measures 15.3 mm, it spans ~16 neural arch-like elements (~eight vertebral segments16) and is straight, without an externally differentiated cardiac and pyloric part. The preserved segment seems to correspond to less than
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